Zn-regulated GTPase metalloprotein activator 1 modulates vertebrate zinc homeostasis

Zinc (Zn) is an essential micronutrient and cofactor for up to 10% of proteins in living organisms. During Zn limitation, specialized enzymes called metallochaperones are predicted to allocate Zn to specific metalloproteins. This function has been putatively assigned to G3E GTPase COG0523 proteins,...

Celý popis

Uloženo v:
Podrobná bibliografie
Vydáno v:Cell Ročník 185; číslo 12; s. 2148
Hlavní autoři: Weiss, Andy, Murdoch, Caitlin C, Edmonds, Katherine A, Jordan, Matthew R, Monteith, Andrew J, Perera, Yasiru R, Rodríguez Nassif, Aslin M, Petoletti, Amber M, Beavers, William N, Munneke, Matthew J, Drury, Sydney L, Krystofiak, Evan S, Thalluri, Kishore, Wu, Hongwei, Kruse, Angela R S, DiMarchi, Richard D, Caprioli, Richard M, Spraggins, Jeffrey M, Chazin, Walter J, Giedroc, David P, Skaar, Eric P
Médium: Journal Article
Jazyk:angličtina
Vydáno: United States 09.06.2022
Témata:
ISSN:1097-4172, 1097-4172
On-line přístup:Zjistit podrobnosti o přístupu
Tagy: Přidat tag
Žádné tagy, Buďte první, kdo vytvoří štítek k tomuto záznamu!
Abstract Zinc (Zn) is an essential micronutrient and cofactor for up to 10% of proteins in living organisms. During Zn limitation, specialized enzymes called metallochaperones are predicted to allocate Zn to specific metalloproteins. This function has been putatively assigned to G3E GTPase COG0523 proteins, yet no Zn metallochaperone has been experimentally identified in any organism. Here, we functionally characterize a family of COG0523 proteins that is conserved across vertebrates. We identify Zn metalloprotease methionine aminopeptidase 1 (METAP1) as a COG0523 client, leading to the redesignation of this group of COG0523 proteins as the Zn-regulated GTPase metalloprotein activator (ZNG1) family. Using biochemical, structural, genetic, and pharmacological approaches across evolutionarily divergent models, including zebrafish and mice, we demonstrate a critical role for ZNG1 proteins in regulating cellular Zn homeostasis. Collectively, these data reveal the existence of a family of Zn metallochaperones and assign ZNG1 an important role for intracellular Zn trafficking.
AbstractList Zinc (Zn) is an essential micronutrient and cofactor for up to 10% of proteins in living organisms. During Zn limitation, specialized enzymes called metallochaperones are predicted to allocate Zn to specific metalloproteins. This function has been putatively assigned to G3E GTPase COG0523 proteins, yet no Zn metallochaperone has been experimentally identified in any organism. Here, we functionally characterize a family of COG0523 proteins that is conserved across vertebrates. We identify Zn metalloprotease methionine aminopeptidase 1 (METAP1) as a COG0523 client, leading to the redesignation of this group of COG0523 proteins as the Zn-regulated GTPase metalloprotein activator (ZNG1) family. Using biochemical, structural, genetic, and pharmacological approaches across evolutionarily divergent models, including zebrafish and mice, we demonstrate a critical role for ZNG1 proteins in regulating cellular Zn homeostasis. Collectively, these data reveal the existence of a family of Zn metallochaperones and assign ZNG1 an important role for intracellular Zn trafficking.Zinc (Zn) is an essential micronutrient and cofactor for up to 10% of proteins in living organisms. During Zn limitation, specialized enzymes called metallochaperones are predicted to allocate Zn to specific metalloproteins. This function has been putatively assigned to G3E GTPase COG0523 proteins, yet no Zn metallochaperone has been experimentally identified in any organism. Here, we functionally characterize a family of COG0523 proteins that is conserved across vertebrates. We identify Zn metalloprotease methionine aminopeptidase 1 (METAP1) as a COG0523 client, leading to the redesignation of this group of COG0523 proteins as the Zn-regulated GTPase metalloprotein activator (ZNG1) family. Using biochemical, structural, genetic, and pharmacological approaches across evolutionarily divergent models, including zebrafish and mice, we demonstrate a critical role for ZNG1 proteins in regulating cellular Zn homeostasis. Collectively, these data reveal the existence of a family of Zn metallochaperones and assign ZNG1 an important role for intracellular Zn trafficking.
Zinc (Zn) is an essential micronutrient and cofactor for up to 10% of proteins in living organisms. During Zn limitation, specialized enzymes called metallochaperones are predicted to allocate Zn to specific metalloproteins. This function has been putatively assigned to G3E GTPase COG0523 proteins, yet no Zn metallochaperone has been experimentally identified in any organism. Here, we functionally characterize a family of COG0523 proteins that is conserved across vertebrates. We identify Zn metalloprotease methionine aminopeptidase 1 (METAP1) as a COG0523 client, leading to the redesignation of this group of COG0523 proteins as the Zn-regulated GTPase metalloprotein activator (ZNG1) family. Using biochemical, structural, genetic, and pharmacological approaches across evolutionarily divergent models, including zebrafish and mice, we demonstrate a critical role for ZNG1 proteins in regulating cellular Zn homeostasis. Collectively, these data reveal the existence of a family of Zn metallochaperones and assign ZNG1 an important role for intracellular Zn trafficking.
Author Munneke, Matthew J
Monteith, Andrew J
Edmonds, Katherine A
Beavers, William N
Skaar, Eric P
DiMarchi, Richard D
Thalluri, Kishore
Caprioli, Richard M
Rodríguez Nassif, Aslin M
Wu, Hongwei
Krystofiak, Evan S
Perera, Yasiru R
Murdoch, Caitlin C
Petoletti, Amber M
Drury, Sydney L
Kruse, Angela R S
Chazin, Walter J
Weiss, Andy
Jordan, Matthew R
Spraggins, Jeffrey M
Giedroc, David P
Author_xml – sequence: 1
  givenname: Andy
  surname: Weiss
  fullname: Weiss, Andy
  organization: Department of Pathology, Microbiology, and Immunology, Vanderbilt Institute for Infection, Immunology and Inflammation, Vanderbilt University Medical Center, Nashville, TN 37232, USA
– sequence: 2
  givenname: Caitlin C
  surname: Murdoch
  fullname: Murdoch, Caitlin C
  organization: Department of Pathology, Microbiology, and Immunology, Vanderbilt Institute for Infection, Immunology and Inflammation, Vanderbilt University Medical Center, Nashville, TN 37232, USA
– sequence: 3
  givenname: Katherine A
  surname: Edmonds
  fullname: Edmonds, Katherine A
  organization: Department of Chemistry, Indiana University, Bloomington, IN 47405, USA
– sequence: 4
  givenname: Matthew R
  surname: Jordan
  fullname: Jordan, Matthew R
  organization: Department of Chemistry, Indiana University, Bloomington, IN 47405, USA; Department of Molecular and Cellular Biochemistry, Indiana University, Bloomington, IN 47405, USA
– sequence: 5
  givenname: Andrew J
  surname: Monteith
  fullname: Monteith, Andrew J
  organization: Department of Pathology, Microbiology, and Immunology, Vanderbilt Institute for Infection, Immunology and Inflammation, Vanderbilt University Medical Center, Nashville, TN 37232, USA
– sequence: 6
  givenname: Yasiru R
  surname: Perera
  fullname: Perera, Yasiru R
  organization: Departments of Biochemistry and Chemistry, Center for Structural Biology, Vanderbilt University, Nashville, TN 37240, USA
– sequence: 7
  givenname: Aslin M
  surname: Rodríguez Nassif
  fullname: Rodríguez Nassif, Aslin M
  organization: Departments of Biochemistry and Chemistry, Center for Structural Biology, Vanderbilt University, Nashville, TN 37240, USA
– sequence: 8
  givenname: Amber M
  surname: Petoletti
  fullname: Petoletti, Amber M
  organization: Department of Pathology, Microbiology, and Immunology, Vanderbilt Institute for Infection, Immunology and Inflammation, Vanderbilt University Medical Center, Nashville, TN 37232, USA
– sequence: 9
  givenname: William N
  surname: Beavers
  fullname: Beavers, William N
  organization: Department of Pathology, Microbiology, and Immunology, Vanderbilt Institute for Infection, Immunology and Inflammation, Vanderbilt University Medical Center, Nashville, TN 37232, USA
– sequence: 10
  givenname: Matthew J
  surname: Munneke
  fullname: Munneke, Matthew J
  organization: Department of Pathology, Microbiology, and Immunology, Vanderbilt Institute for Infection, Immunology and Inflammation, Vanderbilt University Medical Center, Nashville, TN 37232, USA
– sequence: 11
  givenname: Sydney L
  surname: Drury
  fullname: Drury, Sydney L
  organization: Department of Pathology, Microbiology, and Immunology, Vanderbilt Institute for Infection, Immunology and Inflammation, Vanderbilt University Medical Center, Nashville, TN 37232, USA
– sequence: 12
  givenname: Evan S
  surname: Krystofiak
  fullname: Krystofiak, Evan S
  organization: Cell Imaging Shared Resource, Vanderbilt University, Nashville, TN 37232, USA
– sequence: 13
  givenname: Kishore
  surname: Thalluri
  fullname: Thalluri, Kishore
  organization: Department of Chemistry, Indiana University, Bloomington, IN 47405, USA
– sequence: 14
  givenname: Hongwei
  surname: Wu
  fullname: Wu, Hongwei
  organization: Department of Chemistry, Indiana University, Bloomington, IN 47405, USA
– sequence: 15
  givenname: Angela R S
  surname: Kruse
  fullname: Kruse, Angela R S
  organization: Departments of Chemistry and Biochemistry, Mass Spectrometry Research Center, Vanderbilt University, Nashville, TN 37235, USA
– sequence: 16
  givenname: Richard D
  surname: DiMarchi
  fullname: DiMarchi, Richard D
  organization: Department of Chemistry, Indiana University, Bloomington, IN 47405, USA
– sequence: 17
  givenname: Richard M
  surname: Caprioli
  fullname: Caprioli, Richard M
  organization: Departments of Chemistry and Biochemistry, Mass Spectrometry Research Center, Vanderbilt University, Nashville, TN 37235, USA
– sequence: 18
  givenname: Jeffrey M
  surname: Spraggins
  fullname: Spraggins, Jeffrey M
  organization: Departments of Chemistry and Biochemistry, Mass Spectrometry Research Center, Vanderbilt University, Nashville, TN 37235, USA; Department of Cell and Developmental Biology, Vanderbilt University, Nashville, TN 37232, USA
– sequence: 19
  givenname: Walter J
  surname: Chazin
  fullname: Chazin, Walter J
  organization: Departments of Biochemistry and Chemistry, Center for Structural Biology, Vanderbilt University, Nashville, TN 37240, USA
– sequence: 20
  givenname: David P
  surname: Giedroc
  fullname: Giedroc, David P
  email: giedroc@indiana.edu
  organization: Department of Chemistry, Indiana University, Bloomington, IN 47405, USA; Department of Molecular and Cellular Biochemistry, Indiana University, Bloomington, IN 47405, USA. Electronic address: giedroc@indiana.edu
– sequence: 21
  givenname: Eric P
  surname: Skaar
  fullname: Skaar, Eric P
  email: eric.skaar@vumc.org
  organization: Department of Pathology, Microbiology, and Immunology, Vanderbilt Institute for Infection, Immunology and Inflammation, Vanderbilt University Medical Center, Nashville, TN 37232, USA. Electronic address: eric.skaar@vumc.org
BackLink https://www.ncbi.nlm.nih.gov/pubmed/35584702$$D View this record in MEDLINE/PubMed
BookMark eNpNkE1LxDAYhIOsuB_6BzxIjl5akzRp06MsugoLelgvXko-3mqXtlmTdEF_vV1dwdPMwMMwzBxNetcDQpeUpJTQ_GabGmjblBHGUsJTQukJmlFSFgmnBZv881M0D2FLCJFCiDM0zYSQvCBshjavfeLhbWhVBItXm2cVAHcQVdu6nXcRmh4rE5u9is5jijtnf9iA9-AjaD96_NX0Br-7DlyIKjThHJ3Wqg1wcdQFerm_2ywfkvXT6nF5u06MEDwmQArJJJeHKcLYDCjXKre8FJnQzNii5pbRsh4z1TWnoDPBhMolFaoujWYLdP3bOy79GCDEqmvC4RPVgxtCxfI8L0lJpRjRqyM66A5stfNNp_xn9fcE-wbuzWN-
CitedBy_id crossref_primary_10_1016_j_bioactmat_2025_08_011
crossref_primary_10_1039_D5QO00298B
crossref_primary_10_1146_annurev_arplant_070623_105324
crossref_primary_10_1007_s00775_025_02112_1
crossref_primary_10_1128_spectrum_02279_25
crossref_primary_10_3390_biom12101494
crossref_primary_10_1155_jnme_6911386
crossref_primary_10_1111_mmi_15117
crossref_primary_10_1016_j_chemosphere_2022_136318
crossref_primary_10_1002_ange_202216917
crossref_primary_10_1016_j_jid_2025_05_041
crossref_primary_10_1007_s11665_022_07653_z
crossref_primary_10_2174_0113895575333766240912162252
crossref_primary_10_1371_journal_ppat_1013209
crossref_primary_10_3390_nu15071703
crossref_primary_10_1128_jb_00395_23
crossref_primary_10_1021_acs_chemrev_4c00264
crossref_primary_10_1099_mgen_0_001153
crossref_primary_10_1111_1751_7915_14257
crossref_primary_10_1073_pnas_2303860120
crossref_primary_10_1093_mtomcs_mfac047
crossref_primary_10_1186_s12967_025_06744_4
crossref_primary_10_1002_advs_202412225
crossref_primary_10_1002_1873_3468_14500
crossref_primary_10_1002_1873_3468_14544
crossref_primary_10_1038_s41467_024_47189_5
crossref_primary_10_1073_pnas_2213630119
crossref_primary_10_1038_s41467_024_55784_9
crossref_primary_10_3389_frbis_2024_1406868
crossref_primary_10_1016_j_tjnut_2025_01_004
crossref_primary_10_1021_jacs_2c08050
crossref_primary_10_1016_j_nantod_2025_102867
crossref_primary_10_1016_j_devcel_2024_12_024
crossref_primary_10_1038_s41598_023_30498_y
crossref_primary_10_1080_20468954_2024_2389765
crossref_primary_10_1016_j_procbio_2022_10_022
crossref_primary_10_1016_j_jbc_2023_103047
crossref_primary_10_3389_fpls_2023_1237722
crossref_primary_10_1128_iai_00422_24
crossref_primary_10_1016_j_polymer_2023_125806
crossref_primary_10_1038_d41586_022_01988_2
crossref_primary_10_1002_rmb2_12644
crossref_primary_10_1016_j_ccr_2025_216942
crossref_primary_10_1080_10408398_2025_2524471
crossref_primary_10_1038_s41467_025_56199_w
crossref_primary_10_1097_TA_0000000000004530
crossref_primary_10_1146_annurev_micro_041522_091507
crossref_primary_10_3390_inorganics12010034
crossref_primary_10_1093_mtomcs_mfad029
crossref_primary_10_3389_fpubh_2022_968045
crossref_primary_10_26599_NR_2025_94907871
crossref_primary_10_1016_j_bbamcr_2024_119723
crossref_primary_10_1002_anie_202216917
crossref_primary_10_3390_jfb13040164
crossref_primary_10_1128_jb_00226_24
crossref_primary_10_1002_chem_202302948
crossref_primary_10_1016_j_bpj_2024_03_010
crossref_primary_10_1016_j_cell_2022_05_012
crossref_primary_10_1038_s41579_025_01213_7
crossref_primary_10_1002_advs_202508280
crossref_primary_10_1039_D4SC01294A
crossref_primary_10_1126_science_adg3297
crossref_primary_10_1038_s41467_023_41896_1
crossref_primary_10_1007_s10439_025_03741_y
ContentType Journal Article
Copyright Copyright © 2022 Elsevier Inc. All rights reserved.
Copyright_xml – notice: Copyright © 2022 Elsevier Inc. All rights reserved.
DBID CGR
CUY
CVF
ECM
EIF
NPM
7X8
DOI 10.1016/j.cell.2022.04.011
DatabaseName Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
MEDLINE - Academic
DatabaseTitle MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
MEDLINE - Academic
DatabaseTitleList MEDLINE - Academic
MEDLINE
Database_xml – sequence: 1
  dbid: NPM
  name: PubMed
  url: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
– sequence: 2
  dbid: 7X8
  name: MEDLINE - Academic
  url: https://search.proquest.com/medline
  sourceTypes: Aggregation Database
DeliveryMethod no_fulltext_linktorsrc
Discipline Biology
EISSN 1097-4172
ExternalDocumentID 35584702
Genre Research Support, Non-U.S. Gov't
Journal Article
Research Support, N.I.H., Extramural
GrantInformation_xml – fundername: NIAID NIH HHS
  grantid: R01 AI101171
– fundername: NIGMS NIH HHS
  grantid: T32 GM109825
– fundername: NIDDK NIH HHS
  grantid: P30 DK058404
– fundername: NIAID NIH HHS
  grantid: R01 AI145992
– fundername: NIGMS NIH HHS
  grantid: R35 GM118157
– fundername: NIDDK NIH HHS
  grantid: T32 DK101003
– fundername: NIAID NIH HHS
  grantid: F32 AI157215
– fundername: NIAID NIH HHS
  grantid: R01 AI150701
– fundername: NIGMS NIH HHS
  grantid: T32 GM131994
GroupedDBID ---
--K
-DZ
-ET
-~X
0R~
0WA
1RT
1~5
29B
2FS
2WC
3EH
4.4
457
4G.
53G
5GY
5RE
62-
6J9
7-5
85S
AAEDT
AAEDW
AAFWJ
AAHBH
AAKRW
AAKUH
AALRI
AAMRU
AAVLU
AAXUO
AAYWO
ABCQX
ABDGV
ABJNI
ABMAC
ABOCM
ACGFO
ACGFS
ACNCT
ACVFH
ADBBV
ADCNI
ADEZE
ADVLN
AEFWE
AENEX
AEUPX
AEXQZ
AFPUW
AFTJW
AGCQF
AGHSJ
AGKMS
AHHHB
AIGII
AITUG
AKAPO
AKBMS
AKRWK
AKYEP
ALMA_UNASSIGNED_HOLDINGS
AMRAJ
APXCP
ASPBG
AVWKF
AZFZN
BAWUL
CGR
CS3
CUY
CVF
DIK
DU5
E3Z
EBS
ECM
EFKBS
EIF
F5P
FCP
FDB
FIRID
HH5
IH2
IHE
IXB
J1W
JIG
K-O
KOO
KQ8
L7B
LX5
M3Z
M41
N9A
NPM
O-L
O9-
OK1
P2P
RNS
ROL
RPZ
SCP
SDG
SDP
SES
SSZ
TAE
TN5
TR2
TWZ
UKR
UPT
WH7
YZZ
ZCA
7X8
ID FETCH-LOGICAL-c554t-e078284884705cd3e14ba6d49535b2cd7f4d219f9531bf41eb3525a6815af9cb2
IEDL.DBID 7X8
ISICitedReferencesCount 78
ISICitedReferencesURI http://www.webofscience.com/api/gateway?GWVersion=2&SrcApp=Summon&SrcAuth=ProQuest&DestLinkType=CitingArticles&DestApp=WOS_CPL&KeyUT=000825024300003&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D
ISSN 1097-4172
IngestDate Sat Sep 27 16:41:30 EDT 2025
Mon Jul 21 05:59:35 EDT 2025
IsDoiOpenAccess false
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 12
Keywords metalloprotein
zf-C6H2
CBWD
ZNG1
metallochaperone
zinc finger
GTPase
zinc
COG0523
METAP1
Language English
License Copyright © 2022 Elsevier Inc. All rights reserved.
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c554t-e078284884705cd3e14ba6d49535b2cd7f4d219f9531bf41eb3525a6815af9cb2
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
OpenAccessLink http://www.cell.com/article/S0092867422004585/pdf
PMID 35584702
PQID 2666909185
PQPubID 23479
ParticipantIDs proquest_miscellaneous_2666909185
pubmed_primary_35584702
PublicationCentury 2000
PublicationDate 2022-06-09
PublicationDateYYYYMMDD 2022-06-09
PublicationDate_xml – month: 06
  year: 2022
  text: 2022-06-09
  day: 09
PublicationDecade 2020
PublicationPlace United States
PublicationPlace_xml – name: United States
PublicationTitle Cell
PublicationTitleAlternate Cell
PublicationYear 2022
References 35918525 - Nature. 2022 Aug;608(7921):38-39. doi: 10.1038/d41586-022-01988-2
35688131 - Cell. 2022 Jun 9;185(12):2013-2015. doi: 10.1016/j.cell.2022.05.012
References_xml – reference: 35918525 - Nature. 2022 Aug;608(7921):38-39. doi: 10.1038/d41586-022-01988-2
– reference: 35688131 - Cell. 2022 Jun 9;185(12):2013-2015. doi: 10.1016/j.cell.2022.05.012
SSID ssj0008555
Score 2.6244278
Snippet Zinc (Zn) is an essential micronutrient and cofactor for up to 10% of proteins in living organisms. During Zn limitation, specialized enzymes called...
SourceID proquest
pubmed
SourceType Aggregation Database
Index Database
StartPage 2148
SubjectTerms Animals
GTP Phosphohydrolases - metabolism
Homeostasis
Metallochaperones - metabolism
Metalloendopeptidases - metabolism
Metalloproteins - genetics
Mice
Zebrafish - metabolism
Zinc - metabolism
Title Zn-regulated GTPase metalloprotein activator 1 modulates vertebrate zinc homeostasis
URI https://www.ncbi.nlm.nih.gov/pubmed/35584702
https://www.proquest.com/docview/2666909185
Volume 185
WOSCitedRecordID wos000825024300003&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D
hasFullText
inHoldings 1
isFullTextHit
isPrint
link http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwpV1LS8NAEF7UKnjx_agvVvAazGM3yZ5ExOrF0kOF4iXsK5hDk9rEgv56ZzYpPQmCl0AgC8tkHt_szM5HyI3iieRCGI9BQutBhMjBpGTsxb6y0uJ89Th3ZBPJcJhOJmLUHbjVXVvl0ic6R20qjWfktxBIIJETEF7uZh8eskZhdbWj0FgnvQigDGp1MllNC0-5Yz3FIitsIwm7SzNtfxcejEN-GIZu1GkQ_A4xXagZ7P53k3tkpwOZ9L7Vin2yZssDstXSTn4dkvFb6c1bDnpr6NN4BJGMTm2DNXg3t6EoKd53WGBCTgM6rYz7tqZI3oyV5sbS76LU9L2a2grwZV3UR-R18Dh-ePY6dgVPA4RoPIvgIAX7ZYnPtYlswJSMDfabchVqk-TMgDvL4T1QOQsg6-Yhl3EacJkLrcJjslFWpT0llAkFyAM8VepHTKZWsFgLk-pIJ76VKu-T66W4MtBelLwsbfVZZyuB9clJK_Ns1o7ZyHDwO-wtPPvD6nOyjb_S9XCJC9LLwXbtJdnUi6ao51dOLeA5HL38AHsdwhA
linkProvider ProQuest
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Zn-regulated+GTPase+metalloprotein+activator+1+modulates+vertebrate+zinc+homeostasis&rft.jtitle=Cell&rft.au=Weiss%2C+Andy&rft.au=Murdoch%2C+Caitlin+C&rft.au=Edmonds%2C+Katherine+A&rft.au=Jordan%2C+Matthew+R&rft.date=2022-06-09&rft.eissn=1097-4172&rft.volume=185&rft.issue=12&rft.spage=2148&rft_id=info:doi/10.1016%2Fj.cell.2022.04.011&rft_id=info%3Apmid%2F35584702&rft_id=info%3Apmid%2F35584702&rft.externalDocID=35584702
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1097-4172&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1097-4172&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1097-4172&client=summon